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Crop Protection 27 (2008) 320329 www.elsevier.com/locate/cropro

Risks of herbicide-resistant rice in India: A review

V. Kumara,, R.R. Bellindera, D.C. Brainardb, R.K. Malikc, R.K. Guptad
b

Department of Horticulture, Cornell University, Ithaca, NY 14853, USA Department of Horticulture, Michigan State University, East Lansing, MI 48824 c CCS Haryana Agricultural University, Hisar, Haryana 125004, India d ICARDA-CAC ofce, P.O. Box 4564, Tashkent-700000, Uzbekistan

Received 16 March 2007; received in revised form 16 April 2007; accepted 3 May 2007

Abstract Herbicide-resistant (HR) rice has the potential to improve the efciency of weed management and facilitate adoption of resource conservation technologies (RCTs) in India. However, several important risks associated with HR rice should be examined before its widespread adoption is encouraged. The greatest risk in the commercialization of HR crops is the potential for transfer of the gene conferring the HR trait to related wild and weedy relatives. This could lead to increased weediness or invasiveness. Gene transfer between cultivated and wild or weedy rice is known to occur and existing scientic literature conrms that HR genes can move from HR rice to wild and weedy relatives forming hybrids. The likelihood of such gene transfer is especially high in India, where cultivated rice and its relatives are sympatrically distributed and their owering times overlap. Such gene ow can impact crop invasiveness, tness of wild species, and the loss of native biodiversity. Additionally, HR rice may contribute to the problems of crop volunteers and evolution of herbicide resistance. Based on existing scientic literature, it appears that these risks are low, but that additional studies are needed to fully assess the potential adverse consequences of widespread adoption of HR rice in India. r 2007 Elsevier Ltd. All rights reserved.
Keywords: Gene ow; Fitness; Wild rice; Oryza sativa; Hybridization; Weediness; Invasiveness; Extinction

1. Introduction Rice is the worlds most important crop and is the staple food for more than half of the population (Khush, 2004). About 90% of rice production and consumption worldwide occurs in Asia (Gealy et al., 2003). In India, about 42 million hectares of rice are grown annually (FAO, 2004). The ricewheat cropping system of the Indo-Gangetic Plains, occupying nearly 13.5 million hectares, is the most important cropping system for food security in the region. At present, sustainability of this cropping system is at risk as yields of both rice and wheat are static and total factor productivity is declining. In India, rice is grown traditionally by transplanting rice seedlings into puddled soils. This method reduces weed competition and water percolation losses (Sanchez, 1973), but repeated puddling leads to degradation of soil physical
Corresponding author. Tel.: +1 607 255 1786; fax: +1 607 255 9998.

E-mail address: vk63@cornell.edu (V. Kumar). 0261-2194/$ - see front matter r 2007 Elsevier Ltd. All rights reserved. doi:10.1016/j.cropro.2007.05.017

properties, contributes to formation of hard pans (Sharma and De Datta, 1985), and delays planting of the succeeding wheat crop (Hobbs and Morris, 1996). Labour and water scarcity, and soil health issues are factors stimulating the switch from transplanted to direct-seeded rice (DSR). In recent years, resource conservation technologies (RCTs) like zero tillage (ZT) and bed planting are being promoted in the ricewheat cropping systems for both rice and wheat to reduce cultivation costs, energy consumption, and to improve soil health and prots. DSR eliminates puddling and does not require continuous submergence, which reduces water consumption. Research is underway to develop non-puddled, at-surface or raised-bed and/or zero-till planting systems for DSR. Weed control is a serious challenge in non-puddled DSR because the initial ush of weeds is no longer controlled by ooding (Baltazar and De Datta, 1992; Olofsdotter et al., 2000). Adoption of herbicide-resistant (HR) rice may overcome the problem of weed management in DSR and facilitate the adoption of RCTs (Malik et al., 2003; Kumar

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et al., in press). Three HR systems have been developed in rice: imidazolinone-, glufosinate-, and glyphosate-resistant varieties (Gealy et al., 2003). Glufosinate- and glyphosateresistant rice were developed through transgenic technologies and convey resistance to these broad-spectrum, nonselective herbicides. Imidazolinone-resistant rice is not a transgene because it was developed through chemically induced seed mutagenesis and conventional breeding and conveys resistance to the imidazolinone group of herbicides (Gealy et al., 2003). Despite the potential benets of HR rice for promoting adoption of RCTs (Kumar et al., unpublished), there are several important risks associated with this technology. Cross-pollination between transgenic crops and sexually compatible wild and cultivated non-transgenic rice cultivars is the major pathway for gene escape (Lu et al., 2003; Scott and Burgos, 2004; Zhang et al., 2004). Crosspollination can either increase or decrease the tness of recipient species resulting in greater weediness or extinction (Ellstrand, 2003). The impacts of transgenic crops may be greater in the centres of origin of crops than elsewhere because wide arrays of wild progenitors, wild species, and land races are present there. The debate about the environmental risks associated with transgenic organisms started with their rst development. By the end of 1980s, a consensus developed that transgenic crops may pose environmental risks. Risk assessment is needed on a case-by-case basis, taking into account the transgene, recipient organism, intended release environment, and the frequency and scale of introduction (Andow et al., 1987; National Research Council (NRC), 1987; Tiedje et al., 1989; Andow and Zwahlen, 2006). Key categories of environmental risks associated with transgenic crops include (1) non-target and biodiversity risks; (2) gene ow and recombination; and (3) evolution of resistance in target organisms (Snow and Moran-Palma, 1997; Wolfenbarger and Phifer, 2000; NRC, 2002; Snow et al., 2005). Non-target and biodiversity risks associated with HR rice are especially critical in India, one of the centres of biodiversity of wild rice. The foremost concern is the possibility of the transgene transfer conferring the resistant trait through gene ow to compatible weedy or wild Oryza species. Hancock (2003) suggested that the environmental risks of many transgenic crops can be assessed from already available information on the biology of the crop, the presence of compatible wild or weedy relatives, and the transgene phenotype. In this paper, we have attempted to summarize possible concerns of HR rice in India. 2. Wild and weedy relatives of rice in India Centres of origin of crops are rich in biodiversity and contain land races with wide arrays of phenotypic diversity, wild progenitors, and wild species (Gepts and Papa, 2003). India has been identied as the centre of origin of rice (DeCandolle, 1886; Vavilov, 1926), and many wild and

weedy relatives are present in rice-growing areas in India. Suh et al. (1997) classied weedy rice from different countries into two distinct groups corresponding to indica and japonica cultivars, each of which were further classied into forms resembling either cultivars or the wild type. Indian weedy rice belonged to group II (indica group similar to wild type) which means that these weedy rice strains may have originated from hybridization between wild and cultivated rice. A critical rst step in the assessment of gene ow and its consequences is identication of cultivated and wild or weedy relatives that can hybridize with HR rice in the region. There are more than 20 wild species in the genus Oryza (Brar and Khush, 1997; Khush, 1997). These are divided into four species complexes (sativa, ofcinalis, ridleyi, and meyeriana) (Aggarwal et al., 1999; Olofsdotter et al., 2000). These species with their genomes and distributions are listed in Table 1. Because O. nivara and O. rupogon share the same genome AA as cultivated rice, HR rice crop can easily cross with them (Olofsdotter et al., 2000). In contrast, other wild species such as O. malamphuzhaensis (BBCC), O. ofcinalis (CC), and Oryza granulata (GG), present in India with genomes different from AA are difcult to cross with cultivated rice (Brar and Khush, 1997). The Western Ghats region of South India is rich in biodiversity of wild Oryza species including O. rupogon, O. nivara, O. granulata, O. malampuzhaensis, and O. ofcinalis (Vaughan and Sitch, 1991; Thomas et al., 2001). The Bhoothathankettu, Parambikulam, and Kuralai forest reserves along the Western Ghats in Kerala have been identied for in situ conservation of these wild rice species by the International Rice Research Institute (Vaughan and Sitch, 1991). In India, O. sativa f. spontanea is considered a weedy species in cultivated rice. In some northwestern states of India (e.g. Haryana and Punjab), wild and weedy relatives are not present, thus, there are very low risks of gene ow from HR rice to wild and weedy species except risks of gene ow from crop to crop. However, in eastern India (e.g. eastern Uttar Pradesh, Bihar, Orissa, Manipur, and West Bengal) and southern India, wild and weedy relatives are common and gene ow may occur from HR rice to these species. 3. Likelihood of gene ow from HR rice Gene ow is the incorporation of genes into the gene pool of one population from one or more other populations (Futuyma, 1998, p. 767). Gene ow is ubiquitous even in self-pollinated crops if compatible species present are sympatrically distributed and their owering times overlap. These two conditions are pre-requisites for gene ow to occur. Geographical distribution data suggest that transgene movement from cultivated rice to wild relatives may occur (Vaughan, 1994; Lu et al., 2003). Wild and cultivated rice are sympatrically distributed in large parts of India (Vaughan et al., 2005). Therefore, gene ow is likely to

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322 V. Kumar et al. / Crop Protection 27 (2008) 320329 Table 1 Genus Oryza: species with their genome and distribution Species Oryza sativa complex O. sativa L. O. nivara Sharma et Shasty O. rupogon Griff. ( O. perennis Moench) O. glaberrima Steud. O. barthii A. Chev. ( O. breviligulata A. Chev. et Roehr) O. glumaepatula Steud. O. longistaminata A. Chev. et Roehr. O. meridionalis Ng Oryza ofcinalis complex O. punctata Kotschy ex. Steud. (2n 24) O. punctata Kotschy ex. Steud. (2n 48) O. minuta J. S. Pesl. ex. C. B. Presl. O. malamphuzhaensis O. eichingeri A. Peter O. ofcinalis Wall. Ex. Watt O rhizomatis Vaughan O. alta Swallen O. grandiglumis (Doell) Prod. O. latifolia Desv. O. australiensis Domin. Oryza meyeriana complex O. granulata Nees et Arn. ex. Watt O. meyeriana (Zoll. et Mor. ex Steud.) Baill. Oryza ridleyi complex O. ridleyi Hook. f. O. longiglumis Jansen Species not included in any complex O. brachyantha A. Chev. et Roehr. O. schlechteri Pilger (2n 48) O. neocaledonica Morat (2n 24) Genome Distribution

AA AA AA AA AA AA AA AA BB BBCC BBCC BBCC BBCC CC CC CCDD CCDD CCDD EE GG GG HHJJ HHJJ FF HHKK ??

Worldwide, cultivated Tropical and subtropical Asia Tropical and subtropical Asia, tropical Australia West Africa, cultivated Africa Central and South America Africa Australia Africa Africa Philippines and Papua New Guinea India South Asia and East Africa Tropical and subtropical Asia, tropical Australia Sri Lanka Central and South America Central and South America Central and South America Tropical Australia South and Southeast Asia Southeast Asia South Asia Irian Java, Indonesia, Papua New Guinea Africa Papua New Guinea New Caledonia

Classied according to species complexes. Reproduced with permission from Annals of Applied Biology, Blackwell Publishing Ltd., Oxford, UK. Source: Olofsdotter et al. (2000).

take place from HR rice in rice-producing areas of India where these wild and weedy relatives overlap. The owering time of wild rice varies signicantly depending on geographical distribution (Lu et al., 2003). A study in China, showed that wild rice, O. rupogon, and two cultivated rice cultivars viz. a late-maturing local variety and an improved variety (Minghui-63) had a signicant overlap in their pollination and owering timing (Lu et al., 2003). Wild rice usually has a protracted owering period at each locality (Lu and Snow, 2005), which creates more favourable conditions for overlap of owering with cultivated rice. Gene ow from HR rice to wild and weedy relatives has been widely studied in the US, Europe, and China (Estorninos et al., 2002; Gealy et al., 2003; Song et al., 2003; Chen et al., 2004; Messeguer et al., 2004; Shivrain et al., 2006). In most of these studies, outcrossing rates were found to be less than 1%. Langevin et al. (1990) observed that the natural hybridization rate can range from 1% to 52%, depending on cultivar type. Outcrossing is

generally higher between Indica cultivars and wild species than with Japonica cultivars (Oka, 1988). Studies on gene ow from rice to weedy or wild rice are reviewed in Gealy et al. (2003), Lu and Snow (2005), and Lu et al. (2003). In addition to gene ow from HR rice to its wild and weedy relatives, gene ow from HR rice to conventional rice cultivars is another risk in India. The contamination of Basmati rice (long grained aromatic rice) by gene ow is a major concern because India is one of the worlds largest exporters. Information on gene ow from crop to crop is important especially if GM rice must be separated from non-GM rice for market acceptability. Messeguer et al. (2001) found 0.050.53% gene ow from HR rice to adjacent plants of non-HR rice counterparts. Rong et al. (2007) found that gene ow from crop to crop was dramatically reduced within a short distance from transgenic rice. For example, gene ow declined from 0.3% at 0.2 m to o0.01% at 6 m from transgenic rice. Gene ow from HR rice to non-HR-rice cultivars has the potential to increase the opportunities

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of subsequent gene ow to wild or weedy relatives (Lu and Snow, 2005). Information on the distance of pollen dispersal is essential for establishing an effective buffer zone to prevent gene escape to wild species and to avoid contamination of non-transgenic rice cultivars. The distance of gene ow is inuenced by environmental factors especially wind speed and direction, ambient temperature, and relative humidity (Jackson and Lyford, 1999; Galan et al., 2000). Song et al. (2003) found gene ow from cultivated rice to O. rupogon at a maximum distance of 43 m. Rice pollen ow has been detected up to 110 m (Song et al., 2004a). Careful monitoring of HR rice is needed even in those areas where wild or weedy relatives are not present because with the adoption of DSR, problems of weedy rice would likely emerge. For example, weedy rice is becoming an acute problem in areas where transplanting is being replaced by DSR such as in Vietnam, Malaysia, SriLanka, Thailand, and Korea (Baki et al., 2000). 4. Effects of HR trait on crop invasiveness Once a transgene is introduced into wild or weedy relatives, its long-term persistence in the environment depends on several factors, including whether the transgene confers a tness benet. The main potential harmful consequences of gene ow include: (1) increased tness of wild relatives and hence evolution of increased weediness or invasiveness; (2) the loss of an effective tool (HR crops) to control closely related weeds; and (3) loss of biodiversity (e.g. increased likelihood of extinction of wild relatives) (Ellstrand et al., 1999; Gepts and Papa, 2003). There are two main pathways by which a transgenic organism or its resistant gene could increase invasiveness in natural ecosystems: self-sustaining populations in the wild or introgression of genes (Wolfenbarger and Phifer, 2000). Crawley et al. (2001) conducted a 10-yr study on the performance of four transgenic crops (oilseed rape, potato, maize, and sugar beet) grown in 12 natural habitats. They found that these transgenic crops were no more invasive or persistent than their conventional counterparts in any of the habitats studied. The HR trait is unlikely to have any additional risks of increasing invasiveness in a natural setting, since most HR traits in crops are considered neutral in the natural environment (Duke and Cerdeira, 2005; Stewart et al., 2003). Current literature suggests that HR crops including rice are no more likely to be invasive in either agricultural or natural settings in the absence of the herbicide than their conventional counterparts (Lavigne et al., 1995; Hails et al., 1997; Snow et al., 1999; Oard et al., 2000; Zhang et al., 2003). Another potential risk associated with the introduction of HR rice is the problem of HR-crop volunteers. A volunteer is a crop plant which grows in the subsequent crop or year in the same eld from the seed loss from harvest of HR crops (Warwick and Stewart, 2005). Rice can be a volunteer weed in the next years rice crop or any

other subsequent crop. Glyphosate and glufosinate are currently used as burn-down herbicides before planting crops in ZT systems. Volunteer HR rice could limit the option of using these herbicides in ZT systems. The presence of HR volunteer rice would require use of other herbicides to control volunteers (Gealy, 2005). HR volunteer rice would also serve as a potential pollen source for dispersal of transgenes to weedy or wild relatives. Volunteer problems will be more challenging in ZT systems and also in Southern India where rice is grown multiple times a year. 5. Effect of HR trait on tness of crop-wild hybrid Most of the studies on tness of crop-wild hybrids have compared tness of conventional crop wild hybrids to their parents. Such studies have been conducted on multiple crops including sorghum (Arriola and Ellstrand, 1997), sunower (Snow et al., 1998), radish (Klinger and Ellstrand, 1994; Snow et al., 2001), rice (Langevin et al., 1990; Song et al., 2004b), canola (Jrgensen et al., 1996; Hauser et al., 1998a, b), and carrot (Hauser, 2002). In these studies, crop-wild hybrids demonstrated enhanced (e.g. Langevin et al., 1990; Klinger and Ellstrand, 1994), reduced (Jrgensen et al., 1996; Hauser et al., 1998b; Snow et al., 1998, 2001), or equal tness (Arriola and Ellstrand, 1997; Song et al., 2004b) compared to wild controls. To more fully evaluate the impact of HR transgenes on tness of wild populations, the tness of HR vs. non-HR crop wild hybrids needs to be considered. Few studies have estimated the tness of HR vs. non-HR crop wild hybrids (rice, Oard et al., 2000; Zhang et al., 2003; sunower, Massinga et al., 2005; and oilseed rape, Snow et al., 1999). Most of these studies found no direct positive or negative impact of the HR transgene on the tness of crop wild hybrids. Different transgenes can have different impacts on tness. Transgenes, which have the potential to release weedy or wild populations from constraints that restrict or limit their tness, can exacerbate weediness and invasiveness (Lu and Snow, 2005). For example, Snow et al. (2003) demonstrated that the presence of an insect-resistant (Bt) transgene increased the fecundity of wild sunower compared to its non-transgenic counterparts. Ecological theory suggests that HR traits have some costs associated with them in the absence of herbicide use (Bergelson and Purrington, 1996). These costs may be because of pleiotropy, insertion sites within the genome (linkage to deleterious alleles), and physiological costs of resistant traits (Bergelson et al., 1996). Fitness costs have been demonstrated for resistance to many herbicides including triazines (Bergelson et al., 1996; Holt and Thill, 1994; Gressel, 2002). However, HR traits are not always costly in the absence of herbicides and in some cases may even enhance tness (Plowman et al., 1999). For example, no tness cost was found to be associated with glufosinateresistant genes in weedy Brassica rapa introgressed from

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glufosinate-resistant oilseed rape (Snow et al., 1999). Plowman and Richards (1997) reported that susceptible (S) biotypes of B.rapa outperformed the resistant (R) biotypes at high light and medium temperatures, whereas at low light and high temperatures, R-biotypes outcompeted S-biotypes. If the resistance trait has a negative effect, wild relatives may be reduced in size (demographic swamping) (Levin et al., 1996; Wolfe et al., 2001), and can lead to extinction (Ellstrand and Elam, 1993; Levin et al., 1996). Alternatively if a resistance trait has a positive effect, the hybrid may become invasive (Tiedje et al., 1989). Pollen-mediated gene ow from crops to wild relatives is implicated in the evolution of weediness and extinction risk in several crops, including rice (Ellstrand et al., 1999). The relative tness effects of HR traits depend at least in part on the mechanism of resistance. For target-site-based herbicide resistance, an associated decrease in plant tness in the absence of herbicide is well documented for triazine herbicides (Holt and Thill, 1994; Gressel, 2002). This is because target-site mutation decreased the efciency of photosynthetic electron ow through photosystem II, and consequently reduced tness. In contrast to the triazines, resistance to ALS inhibiting herbicides does not consistently reduce plant tness (Holt and Thill, 1994; Tranel and Wright, 2002). For example, Mallory-Smith et al. (1992) and Thompson and Thill (1992) found no evidence for decreased tness in sulphonylurea-resistant (R) biotypes of Kochia scoparia compared to susceptible (S) biotypes originating from Kansas and North Dakota. Dyer et al. (1993) found that sulphonylurea R-biotypes from Montana germinated faster than S-biotypes but it is unclear what effect, if any, this has on relative tness. Christoffoleti and Westra (1991) reported that ALS R-biotypes from Colorado appeared less competitive than S-biotypes. Potential tness advantages (e.g. rapid germination under cool temperatures) in ALS R-biotypes have been demonstrated by many authors (Dyer et al., 1993; Thompson et al., 1994; Eberlein et al., 1999). However, Bergelson et al. (1996) demonstrated tness costs associated with the ALS inhibitor resistance gene in Arabidopsis thaliana. For nontarget-site-based resistance, costs may be associated with increased allocation of resources for production of novel detoxifying enzymes (Coley et al., 1985; Herms and Mattson, 1992). In this case, tness costs depend on whether enzyme production is constitutive or induced by herbicide applications (Strauss et al., 2002). Because glyphosate- and glufosinate-resistant crops exploit the detoxication strategy (non target-based) (Tan et al., 2006), tness costs may be associated with these traits. However, Snow et al. (1999) reported no tness cost of the transgenic glufosinate-resistant trait introgressed from Brassica napus into weedy B. rapa. In contrast, glyphosate-tolerant Ipomoea purpurea biotypes from Georgia, USA, were less t and produced 35% fewer seeds than S-biotypes in the absence of glyphosate (Baucom and Mauricio, 2004).

The effects of HR traits on the tness of wild or weedy relatives of rice are summarized in Table 2. In all the tness-related studies conducted so far on rice, the HR trait had no effect on hybrid tness in the absence of herbicide. For example, glufosinate-resistant rice red-rice hybrids and subsequent progeny were statistically similar to their susceptible counterparts in certain vegetative (plant vigour, plant density) and reproductive traits (dormancy and seed production) (Oard et al., 2000; Zhang et al., 2003). Cultivated rice (non HR) wild rice (O. rupogon) or red-rice hybrids were taller and had more tillers at the vegetative stage (Langevin et al., 1990; Song et al., 2004b) but had lower seed set and pollen viability than their wild parent (Song et al., 2004b).

6. Effect of the herbicide resistance trait on native biodiversity Transgene ow can cause the erosion of genetic diversity in wild populations (Ellstrand, 2003). The possible impacts of transgenic HRCs on biodiversity may be caused by (1) leakage of resistant traits into related wild populations by hybridization; (2) acquisition of tness traits by wild relatives through introgression with the HRC; and (3) impacts on non-target species (Thompson et al., 2003). The possible effects of gene ow on the loss of biodiversity may occur through genetic assimilation, in which crop genes replace the genes in wild species through continuous hybridization or through demographic swamping, whereby hybrids are less fertile than their wild types and hence the population of wild plant shrinks in size (Levin et al., 1996; Wolfe et al., 2001). The populations which are small and rare are at higher risk and can be lost by swamping. Swamping has been implicated in the near extinction of O. rupogon ssp. formosana, a wild relative of rice in Taiwan (Kiang et al., 1979 cited in Ellstrand et al., 1999). To our knowledge, no studies have been conducted on the long-term effects of HR traits on native biodiversity or effects on rare taxa. Gene ow poses problems in in situ conservation of wild biodiversity. Wild species and landraces are critical sources of genetic diversity for plant breeding (Braun and Bennett, 2001; Ellstrand, 2003). The forested hills of the Jeypore tract of Orrisa and Western Ghats region of South India are highly rich in native rice diversity (Vaughan and Sitch, 1991; Thomas et al., 2001). Other states where genetic diversity is rich and varied include: Uttar Pradesh, Bihar, West Bengal, Madha Pradesh, and many South Indian States. In Koraput district of Orrisa alone, scientists identied about 1500 rice land races (Richharia and Govindaswami, 1990). In Jeypore, native rice cultivars have fallen from 1750 to about 150 due to use of commercial cultivars. HR rice, therefore, has the potential to impact the in situ conservation of wild biodiversity, especially if transgenes confer any tness advantage or penalty.

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V. Kumar et al. / Crop Protection 27 (2008) 320329 Table 2 Effect of transgenic HR traits on the relative tness of rice-wild/weedy hybrid Hybrid classication F1 hybrid Parents Traits studied Hybrid outcomes Conclusion Reference 325

Cultivated rice (non-HR) red rice Cultivated rice (non-HR) wild rice (O. rupogon)

Biomass production Whole life history

Ricered-rice hybrids demonstrated enhanced vegetative vigour, and hence to their total tness 1. Slightly inferior at sexual reproduction stage (lower seed set and pollen viability) 2. Superior (hybrid vigour) at vegetative stage (plant height and number of tillers) Overall performance similar to their wild parents

Hybrids more t

Langevin et al. (1990) Song et al. (2004b)

F1 hybrid

No tness advantage

F1 hybrid and F2 population

Cultivated rice [both transgenic HR (glufosinateresistant) and nonHR] red rice

Transgenic and non-transgenic-red-rice hybrids were tall compared to parental lines

HR trait (BAR gene) did not improve tness or seed fecundity in F1 hybrid or subsequence progeny

Zhang et al. (2003)

Seed fertility reduced in both transgenic and nontransgenic hybrids F2 population Cultivated rice [both transgenic HR (glufosinateresistant) and nonHR] red rice (four biotypes) Vegetative and reproductive both No signicant difference seen in plant vigour, density, or seed dormancy HR trait did not increase or decrease tness value for reproductive success traits such as dormancy and seed production Oard et al. (2000)

Plant height and maturity: Louisiana (LA) populations derived from transgenic lines were signicantly different from those developed from non-transgenic lines. Conversely, value for these traits was not greater than those found in red-rice biotypes Seed shattering: Arkansas (AR) populations derived from transgenic rice lines had higher shattering than population from non-transgenic rice lines but no signicant difference was observed among LA population. However, seed shattering value was not greater than that found in red-rice biotypes

Lu and Snow (2005) proposed that gene ow from transgenic rice will not threaten the genetic diversity of wild relatives any more than gene ow from conventional varieties. Moreover, the tness effects of the HR trait are likely to be small compared to other traits like disease, insect, or drought resistance, since the HR trait in HRCs is considered neutral in the absence of herbicide use. 7. Herbicide resistance in weeds Another potential concern with HRCs is evolution of HR weeds due to increased reliance on herbicides for weed control (Owen and Zelaya, 2005). At present, about 310 resistant biotypes have evolved resistance to 19 different target-site chemistries (Heap, 2006). Evolution of herbicide resistance in weeds through selection pressure poses greater risks than development of resistance through gene ow in related species in those HRCs in which frequency of interspecic hybridization and subsequent introgression is

often low (Beckie et al., 2001; Warwick et al., 2004). Development of resistance in weeds to glyphosate was considered unlikely because of its unique site of action. However, evolved glyphosate resistance was observed in Conyza canadensis 3 years after adoption of glyphosateresistant soybean (VanGessel, 2001). Other weed species that also have evolved resistance to glyphosate include: Lolium rigidum in Australia (Powles et al., 1998), Eleusine indica in Malaysia (Lee and Ngim, 2000), and L. multiorum in Chile (Perez and Kogan, 2003). Recently, glyphosate-resistant Amaranthus palmeri was conrmed in Georgia (Culpepper et al., 2006). Evolution of resistance in weeds to ALS-inhibitor herbicides has been reported more frequently than any other herbicides. This is because they exert strong selection pressure as a result of high activity on susceptible biotypes as well as persistent soil residual activity (Tranel and Wright, 2002). It is estimated that mutation frequency for ALS-herbicide resistance in O. sativa could be 108109

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(Olofsdotter et al., 2000), much lower than normal mutation frequency for ALS inhibitors in other plants, which is estimated at about 106 (Chaleff and Day, 1984). Hence, resistance development to ALS-inhibiting herbicides (IMI-rice) in weedy rice through selection pressure might require more time than other species (Olofsdotter et al., 2000). Gene ow from IMI rice to weedy rice could, however, hasten resistance development in weedy rice. The risks of development of herbicide resistance can be minimized with an integrated weed management approach. Long-term studies conducted by Powles et al. (1997) on the management of HR L. rigidum in Australia have conrmed that IWM can be very effective in management of HR weeds. IWM strategies include crop rotation, rotation of herbicides with different modes of action, herbicide mixtures, using the concept of critical period of weed control, adjusting cultural practices, use of HR rice, mechanical weeding, and use of stale seed bed practices. Beckie (2006) recently reviewed both herbicide (sequences and rotation, mixtures, application rate, site-specic application, and use of HRCs) and non-herbicide (crop rotation, cultural practices, and mechanical practices decision support system) tactics for the management of HR weeds. Integrating non-herbicide weed management practices with selective use of herbicides have mitigated the evolution and spread of HR weeds. 8. Conclusions and future research needs The foremost concern associated with the commercialization of HR rice is transfer of the HR trait to wild and weedy relatives via gene ow. Gene ow from HR rice through crop-to-wild or weedy relatives is possible because in large parts of India many wild and weedy relatives of rice are sexually compatible, have sympatric range, and overlapping owering times. However, the consequences of escaped HR transgenes are largely unknown. Resistant traits can potentially reduce the native biodiversity either by increased weediness (if the resistant trait confers a tness benet) or by increased likelihood of extinction of wild relatives (if the resistant trait confers tness penalty). Based on currently published data, these potential risks are relatively low because the HR traits have not shown any tness penalty or benets to wild species in the absence of herbicide and HR trait in HRCs is considered neutral. There will be minimal risk in the northwestern Indian states of Punjab and Haryana as there are no wild or weedy relatives of rice present, but direct seeding in rice would potentially promote the problem of HR-weedy rice. The risks of gene ow and their consequences are higher in eastern and southern Indian states. Full assessment of the risks of HR rice would benet from increased research in the following critical areas: (1) Information on the current geographic distribution of cultivated rice and wild rice species and their time of owering needs to be updated to predict the likelihood

(2)

(3)

(4)

(5)

of gene escape from HR rice to wild and cultivated rice. There is a need for morphological and phenological characterization of the wild rice present in India. Further evaluation of hybridization rates between HR rice and its wild and weedy relatives present in India to determine the compatibility differences and heterosis potentials of hybrids between wild relatives and HRrice cultivars. Information on the frequency and distance of outcrossing from HR rice to wild/weedy relatives and to conventional rice cultivars including basmati type under Indian conditions. This information will help in mitigating risks associated with gene ow by using spatial isolation between HR rice from wild relatives and conventional cultivars. More research on the consequences of gene ow to improve understanding of the effects of different HR traits on the tness of wild relatives under Indian conditions. Research for the development of integrated management strategies to minimize the risk of development of herbicide resistance in weed populations in India. Regionally based agronomic research is needed to develop best management practices for weed control and resistance management (Gealy et al., 2003).

Acknowledgments We thank Vinod K. Shivrain and Dr. Roger Turner for valuable comments on an earlier draft of the manuscript.

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